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Prey Capture Behavior in the Blue-Tongued Skink, Tiliqua Scincoides

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Prey Capture Behavior in the Blue-Tongued Skink, Tiliqua Scincoides loomal of Herpeiolog'l' Vol. 33, No.3, pp. 362-369, 1999 Copyright 1999 Socety for the Study of Amphibians and Reptiles Prey Capture Behavior in the Blue-tongued Skink, Tiliqua scincoides TAMARA 1. SMITH,1 KENNETH V, KARDONG,I,2 AND VINCENT 1. BELS3 'Department of Zoology, Washington State University, Pullman, Washington 99164-4236, USA and E-mail: [email protected] 3Institute of Agriculture, Agronomic Center of Applied Research in Hainut, rue paul PastUT, 11, B-7800 Ath, Belgium ABSTRACT.-Squamate prey capture evolved in two general directions; one toward an emphasis upon lingual prehension and the other toward an emphasis upon jaw prehension. In basal squamates (lguania), lingual prehension characterizes prey capture. All other squamates (Scleroglossa) tend to use their jaws for prey prehension and the role of the tongue as a prehensile organ is reduced. However, within some scierogJossan lizards, lingual and jaw modes of prehension are present Selection of a distinct prehension mode during a feeding bout in these lizards has been hypothesized to be related to prey size. To test for the presence of lingual prehension and correlation with prey size, we examined feeding behavior in the blue-tongued skink, Tiliqua scincoides using two prey types (mealworm and cricket>. We confirmed that this skink uses both lingual and jaw modes of prehension with accompanying characteristic jaw kinematic profiles. With crickets, only jaw prehension was exhibited, but both modes were used when feeding on equivalently sized prey, mealworms. Consequently, prehension mode is not exclusively elicited by prey size. We, therefore, hypoth­ esize that selection of prehension modes, lingual or jaws, in these basal scleroglossans also includes prox­ imate factors related to prey behavior. The tongue of iguanian lizards is used in prey ceptions. In herbivorous iguanians, the tongue capture (Throckmorton, 1976; Smith, 1984; may be used to draw the leaf or food to the Schwenk and Throckmorton, 1989; Bell, 1990; mouth and crop it with the jaws. But occasion­ Bels and Goosse, 1990; Kraklau, 1991; Delheusy ally the jaws are used to grasp and tear vege­ and Bels, 1992), an ancestral state for Squamata tation. In the sister group, Sphenodon, jaw pre­ (Schwenk, 1988; Schwenk and Throckmorton, hension is used to secure large prey (Gorniak et 1989). But within the more derived scleroglos­ aI., 1982; Schwenk and Throckmorton, 1989). sans, there is a tendency for the tongue to be­ However, SphenodOl1 and all iguanians use lin­ come specialized for chemoreception (Burg­ gual prehension for small prey (Schwenk and hardt, 1970; Schwenk, 1988, 1993), and its role Throckmorton, 1989). in prey capture lost as the jaws assume the ma­ Exceptions to the general pattern of prehen­ jor role in prehension. Each feeding mode, lin­ sion by means of jaws also exist for scleroglos­ gual and jaw prehension, is accompanied by a sans. Trachydosaurus rugosus (Scincidae), feeding characteristic kinematic profile (Fig. 1) (Bramble on snails, initially contact the prey with the and Wake, 1985; Schwenk and Throckmorton, tongue which drew the snail a short distance 1989; Goosse and Bels, 1992; Urbani and Bels, across the substrate until the jaws secured the 1995; Bels and Kardong, unpubl. data). For ig­ prey (Gans et aI., 1985). The snail is never lifted uanians, the kinematic pattern accompanying by the tongue and carried into the mouth, a be­ tongue prehension consists of four stages. Jaw havior interpreted as kinematically distinct from opening begins with a slow open I (SOl), fol­ that recorded in iguanians (Schwenk and lowed by a slower, slow open II stage (SOIl), Throckmorton, 1989). In another scleroglossan, and ends with a fast open stage (FO) as the Zonosaurus laticaudatus (Corydiylidae), jaws were tongue projects from the mouth (Schwenk and used with large prey, but tongue use was used Throckmorton, 1989; Bels et aI., 1994). During with small prey; it was concluded that the jaw closing, the jaws rapidly close (FC) (Fig. 1A). kinematic profiles accompanying tongue use For some scleroglossans, the kinematic profile represented an ancestral prehension profile as accompanying jaw prehension consists of a fast observed in iguanian lizards (Urbani and Bels, open (FO) and fast close stage (FC), and the 1995). tongue does not protrude from the mouth (Fig. While jaw prehension is the sole mode of cap­ IB). ture in derived scleroglossans, even with very .~ In general, lingual prehension characterizes small prey (Smith, 1982, 1986; Schwenk and the iguanian clade, and jaw prehenSion charac­ Throckmorton, 1989), there is evidence that terizes the scleroglossan clade, but there are ex- tongue use is present in some groups of basal scleroglossan lizards and choice of feeding 2 Corresponding Author. mode is related to size of the prey (Urbani and LIZARD FEEDING 363 A B .o· SOl SOIl Fa Fe FO Fe FIG. 1. Characteristic kinematic profile (modified from Bramble and Wake, 1985). (A.) The kinematic pattern accompanying lingual prehension consists of four stages. Jaw opening begins with a slow open I (501) followed by a slower, slow open II stage (SOD), and ends with a fast open stage (Fa) as the tongue projects from the mouth. During closing, the jaws rapidly close (FC). (B.) The kinematic profile accompanying jaw prehension consists of a fast open (Fa) and fast close stage (FC), and the tongue does not project from the mouth. Bels, 1995). It has been hypothesized that when tive bred blue-tongued skinks, Tiliqua scincoides, lingual prehension is present in a species, a obtained from a commercial dealer. All had switch in prehension mode is mediated by the been in captivity over six months before feeding size ratio of predator to prey, a consequence of trials were initiated. Each lizard was isolated in changing surface area of the tongue relative to a terrarium (100cm X 50cm X 50cm) before the prey size (Bramble and Wake, 1985; filming. An incandescent bulb and two True­ Schwenk and Throckmorton, 1989; Urbani and Lite tubes provided the animal with a temper­ Bels, 1995). Consequently, the prehension mode ature of 21 C (night) and 29 C (d). The relative is largely determined by the wet adhesive prop­ humidity was maintained near 70%. Animals erties of the tongue relative to prey size, such were conditioned to feed on the cage floor in that, as the prey becomes larger the tongue loses front of a reference grid (10 X 10 mm). In film­ its effectiveness and the lizard must capture ing trials the prey consisted of equivalently prey using jaw prehension (Bramble and Wake, sized mealworm larvae (mean size: 23 :!:: 11 1985; Schwenk and ThrockulOrton, 1989). The mm) and crickets (mean size: 31 :!:: 8mm). significance of lingual prehension in some spe­ Feeding Trials.-For high-speed cinematogra­ cies of scleroglossans is disputed as whether it phy, four adult blue-tongued skinks, Tiliqua represents an isolated occurrence, or character­ scincoides (SVL: 27.11 :!:: 8.0cm) were filmed at izes these species as functional intermediates 100 frames/sec using Eastman Ektachrome between ancestral iguanian lizards and more high-speed 7250 tungsten 16 mm film, using a derived scleroglossans (Schwenk and Throck­ photosonic 1 PL camera under two 1000w tung­ morton, 1989). sten photoflood lights. At the initiation of a To characterize the relationships between mealwonn feeding trial, a preweighed and mea­ prey type and prehension mode, we exarn.ined sured mealwonn was placed in front of the liz­ feeding behavior in a scleroglosan species, the ard using long forceps. The camera was started blue-tongued skink, Tiliqua scincoides, which we and the ensuing predatory behavior filmed. For found to use both lingual and jaw prehension. a cricket feeding trial, one preweighed and mea­ We determined prehension mode when pre­ sured cricket was tied to the end of a line and sented with two prey types (mealwonns and placed on the surface in front of the lizard. A crickets) and examined whether or not the pre­ hension modes were correlated with prey size total of 44 mealwonn feeding trials were filmed. alone. Of these, 21 trials were of feeding in which the head of the skink did not tum and remained at MATERIALS AND METHODS right angles to the camera. These favorable Tiliqua scincoides is a scleroglossan lizard views were used for quantitative analysis. A to­ placed within the Scincidae (Estes et al., 1988). tal of 16 cricket feeding trials were filmed, of We adopted the squamate classi£cation present­ which seven trials were true lateral and the ed by Estes et al. (1988) because it is most com­ cricket was captured from the substrate. Frame plete and consistent with squamate monophyly. by frame quantitative analysis of these film se­ This phylogeny recognizes two major clades, quences was perfonned using a Pony-cam the iguania and the scleroglossa. 16mm cine projector. Lizards.-Data were gathered from four, cap­ Qualitative and Quantitative Analysis.-Kine­ 364 T. L. SMITH ET AL. H time-to-close (TC), time from peak gape angle to jaw tips closed; and gape cycle time (GCT), time when jaws first begin to part to jaws tips closed. Maximum head rotation (MHR), the tilt­ ing of the snout downward as measured from the horizontal substrate, was analyzed for Th TP~ missed versus successful prey capture trials. L'I These data were not entirely independent, be­ cause we analyzed several feeding trials from FIG. 2. Digitized points, using natural and distinct markings on the lizard's body: UJ-Upper Jaw, LJ­ one animal. Due to the opportunistic design of Lower Jaw, G-Gape, TH-Throat, E-Eye, H-Head, the study, resulting in uneven sample sizes, any T-Tongue, and P-Prey. Reference bar 2 em. suitable nonparametric test resulted in" the loss of informative data. As a result, each trial was treated as an independent sample and two­ matic profiles of each feeding mode were deter­ tailed student t-tests were used to compare sta­ mined as described elsewhere (Delheusy and tistical variables between prehension modes.
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